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American Journal of Microbiological Research. 2015, 3(3), 93-106
DOI: 10.12691/ajmr-3-3-1
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Removal of Heavy Metals from Aqueous Solutions Using Multi-Metals and Antibiotics Resistant Bacterium Isolated from the Red Sea, Egypt

Mohamed T. Shaaban1, Hassan A.H. Ibrahim2, Ahmed S. Abouhend3, and Khalid M. El-Moselhy3

1Botany Department, Faculty of Science, Menoufia University, Egypt

2Marine Microbiology Laboratory, National Institute of Oceanography and Fisheries, Egypt

3Marine Pollution Laboratory, National Institute of Oceanography and Fisheries, Egypt

Pub. Date: April 28, 2015

Cite this paper:
Mohamed T. Shaaban, Hassan A.H. Ibrahim, Ahmed S. Abouhend and Khalid M. El-Moselhy. Removal of Heavy Metals from Aqueous Solutions Using Multi-Metals and Antibiotics Resistant Bacterium Isolated from the Red Sea, Egypt. American Journal of Microbiological Research. 2015; 3(3):93-106. doi: 10.12691/ajmr-3-3-1


This investigation was incorporate screening for the highest multiple metal and antibiotics resistant marine bacteria at the Northern Red Sea. The two selected bacterial isolates were identified on the basis of phenotypic and genotypic characterization through 16S rDNA gene technique as Alteromonas macleodii and Nitratireductor basaltis. A. macleodii revealed high efficiency in the removal of heavy metals from aqueous solution. Different factors influenced the removal of heavy metals from aqueous solution by A. macleodii such salinity, pH, temperature, biomass and contact time were optimized. The metal removal was greater at the lowest initial metal concentration (50 mg l-1) and decreased with increase in the metal concentration. A. macleodii showed high efficiency in biosorption of different metals in single and multiple metal solution systems. Removal percentage of different metals by A. macleadii in a single metal system at the highest tested metal concentrations (200 mg l-1) reached Pb, 73.8%; Mn, 66%; Fe, 65%; Cu, 64%; Zn, 62%; Ni, 54%; and Cd, 53%. In multiple metal systems containing 30 mg l-1 of different metals, biosorption percentage was Pb, 93%; Fe, 89%; Zn, 55%; Cd, 50%; Cu, 44.5%; Mn, 40% and Ni, 36%. These findings suggest the possibility of using these bacterial isolates for bioremediation of heavy metals from heavy metal contaminated ecosystem.

biosorption heavy metals antibiotics marine bacterium

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[1]  Schindler, P. W. (1991): The regulation of heavy metals in natural aquatic systems. In: Vernet, J. P. (Ed.) Heavy Metals in the Environment. Elsevier, Amsterdam, pp. 95-123.
[2]  Ansari, M. I.; Masood, F. and Malik, A. (2011): Bacterial Biosorption: a technique for remediation of heavy metals. In Microbes and microbial technologies (eds, I. Ahmad et al.), Springer Science+Business Media.
[3]  McKay, G.; Otterburn M. S. and Sweeny, A. G. (1980): Thr removal of colour from effluents using various adsorbents IV. Silica: equilibria and column Studies. Water Res., 14(1): 21-27.
[4]  Miyaji, F.; Masuda, S. and Suyama, Y. J. (2010): Adsorption of Lead and Cadmium Ions from Aqueous Solution with Coal Fly Ash-Derived Zeolite/Sepiolite Composite. The ceramic society of Japan, 118(11): 1062-1066.
[5]  Ajmal, M.; Rao, R. A. K. and Ahmad, R. (2011): Adsorption studies of heavy metals on Tectona grandis: Removal and recovery of Zn (II) from electroplating wastes. J. Disper. Sci. and Tech., 32(6): 851-856.
[6]  Crist, R. H.; Martin, J. R.; Guptill, P. W.; Eslinger, J. M. and Crist, D. R. (1990): Interaction of metals and protons with algae. 2. Ion exchange in adsorption and metal displacement by protons. Envi. Sci. Tech., 24: 337-342.
[7]  Morcos, S. A. (1970): Physical and chemical oceanography of the Red Sea. Oceanogr. Mar. Biol. Ann. Rev., 8: 73-202.
[8]  Murty, T. S. and El-Sabh, M. T. (1984): Weather system storm surges and sea state in the red sea and the Gulf of Aden. Proc. Symp. Coral Reef Envi. Red sea. Jeddah, pp 8-38.
[9]  Ormond, R. F. G. and Edwards, A. (1987): Red Sea Fishes, in: Edwards, A.J. and Head S.M. (eds), Red Sea. Pergamon Press, Oxford, U.K. pp 252-287.
[10]  Strickland, J. D. H. and Parsons, T. R. (1972): A Practical Hand Book of Sea Water Analysis. Fisheries Res. Board Canada Bull., 167, 2nd ed., p. 310.
[11]  APHA (1992): Standard methods for the examination of water and wastewater. 18th ed. American Public Health Association, Washington, DC.
[12]  Grasshoff, K, Kremling, K. and Ehrhardt, M. (1999): Methods of Seawater Analysis, 3 rd edition,Weinheim; New York, Wiley-VCH, p. 600.
[13]  Koroleff, F. (1969): Determination of ammonia as indophenol blue. International Council for the Exploration of the sea (ICES), p8.
[14]  Brown B. E. and Holley M. C. (1982): Metal levels associated with tin dredging and smelting, and their effect upon intertidal reef flats at Ko Phuket, Thailand. Coral Reefs, 1: 131-137.
[15]  Amini, G. H. R. (1998): Heavy metal concentration in surficial sediments from Anzali Wetland, Iran. Water, Air and Soil Poll., 104: 305-312.
[16]  Boniforti, R.; Ferraroli, I. R.; Frigileri, P.; Heltai, D. and Queirazza, G. (1984): Intercomparison of five methods for the determination of trace metals in sea water, Anal. Chim. Acta. 16: 233-46.
[17]  Oregioni, B. and Aston, S.R. (1984): The determination of selected trace metals in marine sediments by flameless/flame atomic absorption spectrophotometry. IAEA Manaco laboratory, Internal Report. Cited from Reference Method in pollution studies N. 38, UNEP. 1986.
[18]  Raja, E. C.; Selvam, S. G. and Omine, K. A. (2009): Isolation, identification and characterization of heavy metals resistant bacteria from sewage. International joint symposium on geodisaster prevention and geoenvironment in asia, 205-211.
[19]  Summers, Α. Ο. and Silver, S. (1972): Mercury resistance in a plasmid-bearing strain of Escherichia coli. J. Bacteriol., 112: 1228-1236.
[20]  Esposito, A.; Pagnanelli, F. and Vegli, F. (2002): PH-related equilibria models for biosorption in single metal systems. Chem. Eng. Sci., 5: 307-313.
[21]  Volesky, B. and Holan, Z. R. (1995): Biosorption of heavy metals. Biotech. Prog., 11: 235-250.
[22]  Bauer, A. W.; Kirby, W. M. M.; Sherris, J. C. and Turck. M. (1966): Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol., 36: 493-496.
[23]  Garrity, G. M.;Brenner, D. J; Krieg, N. R and Staley, J. T (2005): Bergey’s manual of systematic bacteriology. 2nd edition, Vol. 2.
[24]  Hentschel, U.; Schmid, M.; Wagner, M.; Fieseler, L.; Ger- nert, C. and Hacker, J. (2001): Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS J. Micro. Eco., 35: 305-312.
[25]  Pekey, H. (2006): The distribution and sources of heavy metals in Izmit Bay surface sediments affected by a polluted stream. Mar. Poll. Bull., 52(10): 1197-1208.
[26]  De Rore, H.; Top, E.; Houwen, F.; Mergcay, M. and Verstraete, W. (1994): Evolution of heavy metal-resistant transconjugants in a soil environment with a concomitant selective pressure. FEMS Microbiol. Ecol., 14: 263-273.
[27]  Filali, B. K.; Taoufik, J.; Zeroual, Y.; Dzairi, F. Z.; Talbi, M. and Blaghen, M. (2000): Waste water bacteria resistant to heavy metals and antibiotics. Current Microbiology, 41: 151-156.
[28]  Nair, S.; Chandramohan, D. and Bharathi, L. P. A. (1992): Differential sensetivity of pigmented and non-pigmented marine bacteria to metals and antibiotics. Water. Res., 26(4): 431-434.
[29]  Loaic, M.; Olier, R. and Guezennec, J. (1997): Uptake of lead, cadmium and zinc by a novel bacterial exopolysaccharide. War. Res., 31: 1171-1179.
[30]  Takeuchi, M.; Kawahata, H.; Gupta, L. P.; Kita, N.; Morishita, Y.; Ono, Y. and Komai, T (2007): Arsenic resistance and removal by marine and non-marine bacteria. J. Biotech., 127: 434-442.
[31]  Kim, K.; Roh, W. S.; Chang, H.; Nam, Y.; Yoon, J.; Jeon, O. C.; Oh, H. and Bae, J. (2009): Nitratireductor basaltis sp. nov., isolated from black beach sand. International J. Sys. Evolu. Microbio., 59: 135-138.
[32]  Bridge,T. A. M.; White, C. and Gadd, G. M. (1999): Extracellular metal binding activity of the sulphate reducing bacterium Desulfococcus multivorans. Microbiol., 145: 2987-2995.
[33]  Ahmed, N.; Nawaz, A. and Badar, U. (2005): Screening of copper tolerant bacterial species and their potential to remove copper from the environment. Bull. Envi. Contam. Toxi., 74: 219-226.
[34]  Rajkumar, M. and Freitas, H. (2008): Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals, Chemosphere, 71: 834-842.
[35]  Abskharon, R. N. N.; Hassan, S. H. A.; Kabir, M. H.; Qadir, S. A.; El-Rab, S. M. F. G. and Wang, M. H. (2010): The role of antioxidants enzymes of E. coli ASU3, a tolerant strain to heavy metals toxicity, in combating oxidative stress of copper. World J. Microb. Biotech., 26: 241-247.
[36]  Ansari, M. I. and Malik, A. (2007): Biosorption of nickel and cadmium by metal resistant bacterial isolates from agricultural soil irrigated with industrial wastewater. Biores. Tech., 98(3)149-153.
[37]  Wei, G. H.; Fan, L. M.; Zhu, W. F.; Fu, Y. Y.; Yu, J. F. and Tang, M. (2009): Isolation and characterization of the heavy metal resistant bacteria CCNWRS33-2 isolated from root nodule of Lespedeza cuneata in gold mine tailings in China, J. Haz. Mater., 162: 50-56.
[38]  Verma, T.; Srinath, T.; Gadpayle, R. U.; Ramtake, P. W.; Hans, R. K. and Garg, S. K. (2001): Chromate tolerant bacteria isolated from tannery effluent. Biores. Tech., 78: 31-35.
[39]  Pickett, A. W. and Dean, A. C. R. (1976): Antibiotic resistance of cadmium- and zinc-tolerant strains of Klebsiella (Aerobacter) aerogenes growing in glucose-limited chemostat. FEMS Microbio. Letters., 1:165-167.
[40]  Calomiris, J. J.; Armstrong, L. J. and Seidlier, J. R. (1984): Association of Metal Tolerance with Multiple Antibiotic Resistance of Bacteria Isolated from Drinking Water. Appli. Envi. Micro., 47(6): 1238-1242.
[41]  Long, F.; Su, C. C.; Zimmermann, M. T.; Boyken, S. E.; Rajashankar, K. R.; Jernigan, R. L. and Yu, E. W. (2010): Crystal structures of the CusA efflux pump suggest methioninemediated metal transport. Nature, 467: 484-488.
[42]  Volesky, B. (1990): Biosorption of Heavy Metals. CRC Press, Boca Raton, USA.
[43]  Gutnick, D. L. and Bach, H. (2005): Engineering bacterial biopolymers for the biosorption of heavy metals; new products and novel formulation. Appl. Microbial. Biotech., 54: 45l-460.
[44]  Ruiz, G. C.; Tirado, R. V. and Gil, G. B. (2008): Cadmium and zinc removal from aqueous solutions by Bacillus jeotgali: pH, salinity and temperature effects. Biores. Tech., 99: 3864-3870.
[45]  Schiewer, S. and Volesky, B. (1997): Ionic strength and electrostatic effects in biosorption of divalent metal ions and protons. Envi. Sci. Tech. j., 31: 2478-2485.
[46]  Pivovarov, S. (2003): Physico-chemical modeling of heavy metals (Cd, Zn, Cu) in natural environments. Encyclopedia of Surface and Colloid Science, 1-26.
[47]  Schiewer, S. and Wong, M. H., (2000): Ionic strength effects in biosorption of metals by marine algae. Chemosphere, 41: 271-282.
[48]  Masoudzadeh, N.; Zakeri, F.; Lotfabad, T. B.; Sharafi, H.; Masoomi, F.; Zahiri, H. S.; Ahmadian, G. and Noghabi, K. A. (2011): Biosorption of cadmium by Brevundimonas sp. ZF12 strain, a novel biosorbent isolated from hot-spring waters in high background radiation areas. J. Haz. Mater., 197: 190-198.
[49]  Gadd, G. M.; White, C. and DeRome, L. (1998): Heavy metal and radionuclide uptake by fungi and yeasts, in: Norri, P. R. and Kelly D. P. (Eds.), Biohydrometallurgy, Chippenham, Wilts, UK.
[50]  Aksu, Z. and Cagatay, S. S. (2006): Investigation of biosorption of Gemazol Turquise Blue-G reactive dye by dried Rhizopus arrhizus in batch and continuous systems. Sep. Purif. Tech., 48: 24-35.
[51]  Vijayaraghavan, K.; Jegan, J. R.; Palanivelu, K. and Velan, M. (2004): Copper removal from aqueous solution by marine green alga Ulva Reticulate. Elec. J. Biotech., 7(1): 61-71.
[52]  Guibal, E.; Sancedo, I.; Roussy, J. and Le Cloiree, P. (1994): Uptake of uranyl ions by new sorbing polymers: discussion of adsorption isotherms and pH effect. React. Polym., 23: 147-156.
[53]  Selatnia, A.; Boukazoula, A.; Kechid, N.; Bakhti, M. Z.; Chergui, A. and Kerchich, Y. (2004): Biosorption of lead (II) from aqueous solution by a bacterial dead Streptomyces rimosus biomass. Biochem. Eng. J., 19: 127-135.
[54]  Ozdemir, S.; Kilinc, E.; Poli, A.; Nicolaus, B. and Guven, K. (2009): Biosorption of Cd, Cu, Ni, Mn and Zn from aqueous solutions by thermophilic bacteria, Geobacillus toebii sub.sp. decanicus and Geobacillus thermoleovorans sub.sp. stromboliensis: equilibrium, kinetic and thermodynamic studies. Chem. Eng. J., 152: 195-206.
[55]  Vijayaraghavan, V. and Yun, Y.S. (2008): Bacterial biosorbents and biosorption. Biotech. Adv., 26: 266-291.
[56]  Leung, W. C.; Wong, M. F.; Chua, H.; Lo, W.; Yu, P. H. F. and Leung, C. K. (2000): Removal and recovery of heavy metals by bacteria isolated from activated sludge treating industrial effluents and municipal wastewater, Water Sci. Tech., 41: 233-240.
[57]  Al-Garn, S. M. (2005): Biosorption of lead by Gram -ve capsulated and non-capsulated bacteria.Water SA., 31: 789-796.
[58]  Ianis, M.; Sekova, K. and Vasıleva, S. (2006): Copper biosorption by Penicillium cyclopium: equilibrium and modelling study. Biotech. Eq., 20: 195-201.
[59]  Suriya, J.; Bharathiraja, S. and Rajasekaran, R. (2013): Biosorption of heavy metals by biomass of Enterobacter Cloacae isolated from metal-polluted soils. Inter. J. Chem.Tech. Res., 5(3): 1329-1338.
[60]  Malkoc, E. and Nuhoglu, Y. (2005): Investigations of Ni (II) removal from aqueous solutions using tea factory waste. J. Haz. Mater., 127: 120-128.
[61]  Zakeri, F.; Noghabi, K. A.; Sadeghizadeh, M.; Kardan, M.; Masoomi, F.; Farshidpour, M. R. and Atarilar, A. (2010): Serratia sp. ZF03: an efficient radium biosorbent isolated from hot-spring waters in high background radiation areas. Biores. Tech., 101: 9163-9170.
[62]  Weber, W. J. (1985): Adsorption theory, concepts and models, In: Schijko FL (ed) Adsorption Technology: A Step-by-step Approach to process Evaluation and Application. Marcel Dekkar, NY, 1-35.
[63]  Singh, N. and Gadi, R. (2012): Bioremediation of Ni (II) and Cu (II) from wastewater by the nonliving biomass of Brevundimonas vesicularis. J. Envi. Chem. Ecotoxi., 4(8): 137-142.
[64]  Pardo, R.; Herguedas, M.; Barrado E. and Vega, M. (2003): Biosorption of cadmium, copper, lead and zinc by inactive biomass of Pseudomonas putida. Anal. Bioanal. Chem., 376: 26-32.
[65]  Mashitah, M. D.; Yus Azila, Y. and Bhatia, S. (2008): Biosorption of cadmium (II) ions by immobilized cells of Pycnoporus sanguineus from aqueous solution. Biores. Tech., 99: 4742-4748.
[66]  Premuzic, E. T.; Lin, M.; Zhe, L. L. and Gremme, A. M. (1991): Selectivity in metal uptake by stationary phase microbial populations. Arch. Envi. Contam. Toxicol., 20: 234-240.
[67]  Chang, J. S. and Hong, J. (1994): Biosorption of mercury by the inactivated cells of Pseudomonas aeruginosa PU21. Biotech. Bioeng., 44(8): 999-1006.
[68]  Figueira, M. M.; Volesky, B. and Ciminelli, V. S. T. (1997): Assessment of Interference in biosorption of heavy metal. Biotech. Bioeng., 54(4) 344-350.
[69]  Utigikar, V.; Chen, B. Y.; Tabak, H. H.; Bishop, D. F. and Govind, R. (2000): Treatment of acid mine drainage. I. equilibrium biosorption of zinc and copper on non-viable activated sludge. Inter. Biodeteri. Biodeg., 46: 19-28.
[70]  Puranik, P. R. and Paknikar, K. M. (1999): Biosorption of lead, cadmium and zinc by Citrobacter strain MCM B-181: characterization studies. Biotechnol. Prog., 15: 228-237.
[71]  Prashar, S. O.; Beaugeard, M.; Hawari, J.; Bera, P.; Patel, R. M. and Kim, S. H. (2004): Biosorption of heavy metals by red algae (Palmaria palmata). Envi. Tech., 25: 1097-1106.
[72]  Parungao M. M.;Tacata, P. S.;Tanayan, C. R. G and Trinidad, L. C. (2007): Biosorption of copper, cadmium and lead by copper-resistant bacteria isolated from Mogpog River, Marinduque Philip. J. Sci., 136(2): 155-165.